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Inter-site variation in allometry and wood density of glabra Aubl. in Amazonia N. C. Siliprandia, E. M. Nogueiraa, J. J. Toledob, P. M. Fearnsidea and H. E. M. Nascimentoa* aCurso de Pós-graduação em Ciências de Florestas Tropicais, Instituto Nacional de Pesquisas da Amazonia – INPA, Avenida André Araújo, 2936, Petrópolis, CEP 69067-375, Manaus, AM, bCurso de Pós-graduação em Biodiversidade Tropical, Universidade Federal do Amapá – UNIFAP, Rodovia Juscelino Kubitschek, Km 02, Jardim Marco Zero, CEP 68902-280, Macapá, AP, Brazil *e-mail: [email protected]

Received: October 28, 2014 – Accepted: December 18, 2014 – Distributed: February 29, 2016 (With 4 figures)

Abstract The present study aims to compare the allometry and wood density of Goupia glabra Aubl. (Goupiaceae) in two different terra-firme sites in Amazonian forest. A total of 65 ≥ 10 cm DBH was sampled in both sites, with 39 trees in Nova Olinda do Norte (NOlinda, near the Amazon River) and 29 trees in Apuí (near the southern edge of the Amazon forest).

Except for the relationship between DBH (diameter at breast height) and Ht (total height), allometric relationships for

G.glabra differed significantly between sites. Apuí had lower intercept and greater slope for log10 (DBH) versus log10

(Hs – stem height), and, conversely, greater intercept and lower slope for log10 (DBH) versus log10 (Ch – crown height).

The slope differed significantly between the sites for DBH versus dC (crown diameter), with greater slope found for NOlinda. Mean basic wood density in Apuí was 8.8% lower than in NOlinda. Our findings highlight the variation in adaptive strategy of G. glabra due to environmental differences between sites. This is probably because of different canopy-understory light gradients, which result in differentiation of resource allocation between vertical and horizontal growth, which, in turn, affects mechanical support related to wood density. We also hypothesize that differences in soil fertility and disturbance regimes between sites may act concomitantly with light. Keywords: allometric relationships, functional traits, phenotypic plasticity, tropical species.

Variação entre-sítios na alometria e densidade da madeira de Goupia glabra Aubl. na Amazônia

Resumo O presente estudo tem como objetivo comparar a alometria e a densidade da madeira de Goupia glabra em dois diferentes sítios de floresta de terra firme na Amazonia. Um total de 65 árvores com DAP ≥ 10 cm foi amostrado em ambos os sítios, sendo 39 árvores em Nova Olinda do Norte (NOlinda, próximo ao rio Amazonas) e 29 em Apuí (próximo à borda sul da

Amazônia). Exceto para a relação entre o DBH (diâmetro a altura do peito) e a Ht (altura total), as relações alométricas para G. glabra diferiu significativamente entre os sítios. Apuí apresentou menor intercepto e maior inclinação para a relação log10 (DBH) versus log10 (Hs – altura do fuste) e, ao contrário, maior intercepto e menor inclinação para log10

(DBH) versus log10 (Ch – altura da copa). A inclinação diferiu significativamente entre os sítios para DBH versus dC (diâmetro da copa), com maior inclinação encontrada para NOlinda. A densidade básica média da madeira in Apuí foi 8.8% menor do que em NOlinda. Os resultados deste estudo destacam a variação na estratégia adaptativa de G. glabra devido às diferenças ambientais entre os sítios. Isto é provavelmente consequência dos diferentes gradientes de luz o que resulta na diferenciação na alocação de recursos entre o crescimento vertical e horizontal o que, por sua vez, afeta o suporte mecânico relacionado à densidade da madeira. Nós também levantamos a hipótese de que as diferenças em termos de fertilidade e regimes de distúrbios entre os sítios podem agir concomitantemente com o regime de luz. Palavras-chave: relações alométricas, características funcionais, plasticidade fenotípica, espécies arbóreas tropicais.

1. Introduction In tropical forests light is one of the most limiting the tree (height and diameter) and crown size (both vertical resources for tree growth. The ability of a tree to assimilate and horizontal dimensions), i.e., the tree allometry – the light energy depends on the relationships between the size of spatial distribution of its components along the vertical

268 Braz. J. Biol., 2016, vol. 76, no. 1, pp. 268-276 Allometry of an Amazonian tree species axis (King, 1996; Poorter et al., 2006). Since there is a in terms of soil type and light condition. Our central gradient of light availability ranging from a low light hypothesis was that G. glabra would have distinct allometric level in the understory to a high one in the forest canopy, relationships related to environmental site conditions, and allometric differences are expected among tropical tree that this may be reflected in its wood density. species because of their differences in light requirements (Chazdon and Fetcher, 1984). In this sense, low-statured 2. Methods and shade-tolerant understory tree species, which are adapted to low light environments for establishment and 2.1. Research sites growth, tend to have proportionally wider and shallower This study was carried out in two areas of commercial crowns in order to (i) increase their ability to assimilate timber exploitation in the Brazilian Amazon - one located light along the horizontal light gradient and (ii) avoid in the municipality of Apuí, called Fazenda Nova Era self-shedding. Conversely, shade-intolerant pioneer (59°56’ W; 7°18’ S), and the other located in the municipality species, which only grow in gaps and/or are highly light of Nova Olinda do Norte (hereafter termed NOLinda), called demanding, invest proportionally more in height growth, Fazenda Apapazinho (58°22’W; 3°48’S). Both study sites increasing crown depth while reducing crown horizontal are in the state of Amazonas and are about 400 km apart expansion (King, 1996; Thomas, 1996; Sterck et al., 2001; along a north-south gradient (Figure 1). Apuí is located Alves and Santos, 2002). near the southern edge of the Amazon forest in the “arc Interspecific variation in allometry may be related to of deforestation,” while NOlinda is located in central wood density because density correlates with mechanical Amazonia near the Amazon River. support (King, 1981; Niklas, 1993; Putz et al., 1983). At both sites the average annual temperature is about Light-demanding pioneer species in gaps need to invest 27°C and the mean maximum and mean minimum are more in growth to reach the canopy rapidly and to better 31°C and 23°C, respectively, while annual precipitation compete with other tree species. In contrast, shade-tolerant ranges from 2200 to 2300 mm with two distinct seasons species allocate more energy to survival through greater (INMET, 2009, for a 30-year historical series). Precipitation investment in mechanical support. Therefore, there is a is concentrated between December and April, when the tradeoff in biomass allocation (and, by inference, wood mean monthly rainfall is over 200 mm. However, NOlinda is density) due to the different costs of support between these more uniformly wet, whereas Apuí has a more pronounced two extremes. Pioneer trees require less investment in decline in precipitation between June and August. Moreover, wood tissue to sustain their crown, giving them more rapid the sites differ in terms of vegetation, soils and geological growth and lower support costs, whereas shade‑tolerant formation. The predominant vegetation type in Apuí is species invest more in building tissues (and thus have open montane wet forest and the soils are mainly Acrisols higher wood density), decreasing their susceptibility to (red-yellow latosol in the Brazilian system; Santos et al., physical damage, which ultimately results in a greater 2011). In Nova Olinda do Norte, the dominant vegetation survival advantage (Putz et al., 1983; Thomas, 1996; is classified as evergreen lowland tropical moist forest and King et al., 2006; Poorter et al., 2006). the predominant soils are Xanthic Ferralsols (allic yellow Although the patterns of differentiation in architecture latosol in the Brazilian system), which are heavily weathered, and wood density among functional groups of trees are acidic, and very poor in nutrients such as P, Ca, and K. widely recognized, studies assessing the variation in allometry and wood density of a single species growing 2.2. The studied species in different environmental conditions are rare. Individual The genus Goupia is monotypic with just Goupia glabra trees within a given species have been found to have Aubl. (Goupiaceae). G.glabra is a canopy semideciduous lower wood density (Nogueira et al., 2007) and shorter species with ascending branches and cylindrical stem. height for any given diameter (Nogueira et al., 2008a) in The bark is gray, with chipped lengthwise lenticels. The bark southern Amazonia as compared to central Amazonia. is 1 cm thick and comes off in large slabs. G. glabra To our knowledge, the present study is the first to develop has a continuous pattern of flowering and fruiting, but species-specific allometric equations for populations flowering peaks usually occur at the end of the dry season of a species with parameters specific to each of these and fruiting peaks in the early rainy season. The is a subregions. At the community level and at different spatial globose from 3 to 6 mm in diameter. number scales, several studies have shown significant correlations ranges from one to five per fruit. are approximately between wood density and environmental variables that 1.5 mm long and 1 mm wide and are dispersed primarily are affected by variation in altitude, latitude and soils by (Ribeiro et al., 1999; Ferreira and Tonini, 2004). (Wiemann and Williamson, 2002; Muller-Landau, 2004; G. glabra has a wide distribution, occurring from the Baker et al., 2004; Wittmann et al., 2006; Nogueira et al., tropical rainforests of Panama and to Amazonian 2007; Swenson and Enquist, 2007; Slik et al., 2010). terra firme forests. Trees can reach up to 40 m in height and The present study aimed to compare the architectural up to 130 cm in diameter at breast height (DBH), growing features and wood densities of Goupia glabra growing at preferentially either on clayey or well-drained sandy two different sites in terra-firme (not seasonally flooded) soils (Loureiro et al., 1979; Ferreira and Tonini, 2004). lowland forest in Brazilian Amazonia, which differ mainly This species is closely associated with gaps (Loureiro et al.,

Braz. J. Biol., 2016, vol. 76, no. 1, pp. 268-276 269 Siliprandi, N.C. et al.

Figure 1. Location of the municipalities of Apuí and Nova Olinda do Norte and of the forest sites where trees were collected and measured in this study.

1979; Boot, 1996) and is classified as a shade-intolerant 1.3 m, and 2 m and thereafter at 2-m intervals up to the pioneer species (sensu Swaine and Whitmore, 1988). first living branch. All measurements included the bark. Although its wood is heavy, with a density ranging from FF was calculated as the ratio between the bole volume 0.7 to 0.9 g/cm3, G. glabra has relatively high growth calculated by the Smalian formula and cylindrical volume rates in sites with direct sunlight (Loureiro et al., 1979). with a cross-sectional area equal to the measured DBH. Cross sections (5-cm thick) were cut with a chainsaw 2.3. Data collection from each selected tree to determine wood density (Dg) We measured 29 individuals of G. glabra in Apuí and at six positions: 0.5 m, 1 m, 1.3 m, 2 m, middle and top 36 in NOlinda. Individuals with damage to the canopy of the bole. The samples were divided into heartwood, and/or trunk were avoided. At both sites, G. glabra trees sapwood and bark and were weighed in the field on a were collected in logging concessions that encompass portable electronic balance. The volume of each sample 452 ha and 820 ha in Apuí and NOlinda, respectively. was determined immediately after collection to avoid We aimed to obtain a uniform distribution of the number dehydration. The wood samples were fixed on a stylus and of individuals across the DBH size classes at both sites. submerged in a container of water placed on a balance. For each sampled tree ≥ 10 cm DBH, the following According to the Archimedes principle, the volume of data were recorded: DBH, stem height (Hs), total height water displaced by the immersed sample without touching (Ht), crown length (Ch), crown diameter (Cd), commercial the container corresponds to the volume of the sample; volume (Vc), stem form factor (FF), and wood density the amount was recorded in grams, since the density of 3 (Dg). DBH was measured at 1.30 meters above ground water is near 1 g/cm (ASTM, 2002). Subsequently, the level, or just above any buttresses. Hs is the vertical distance samples were placed in paper bags and dried in an oven between the ground level and the height of the lowest living with forced air circulation at 105°C (ASTM, 2002). After branch. Ch was defined as the difference between the first a week, we began weighing each sample at intervals of branch and final height of the crown, and tH is the sum of 24 hours. The average basic wood density for each tree Hs and Ch. Cd was estimated by measuring the horizontal was calculated as the ratio between the dry weight and distance from the trunk to the vertical projection of the the volume of the fresh sample. o crown edge in four compass directions 90 apart. Cd of a tree was calculated by the arithmetic mean of the two 2.4. Data analysis perpendicular directions of the crown. Vc was calculated Dimensional relationships of G. glabra within each by cubic scaling of the bole using the Smalian method site were determined by least square linear regressions. for obtaining the areas of cross sections at 0.5 m, 1 m, Both untransformed and logarithmically-transformed

270 Braz. J. Biol., 2016, vol. 76, no. 1, pp. 268-276 Allometry of an Amazonian tree species

(log10) regressions were performed; the latter substantially no significant difference between sites for DBH versus tH . improved the fit for some relationships. For each allometric However, when DBH was regressed against the two variables relationship, 95% confidence intervals around the intercepts that compose Ht (Hs and Ch), both intercepts and slopes and slopes were calculated using the bootstrap technique were significantly different between sites Figure( 2b, c). (Efron and Tibshirani, 1993). For each site, 1000 bootstrap Furthermore, Apuí had lower intercept and greater slope samples were drawn with replacement. Bootstrapping was for log10 (DBH) versus log10 (Hs), and, conversely, greater also used to indicate a p-value for statistically significant intercept and lower slope for log10 (DBH) versus log10 differences between sites in terms of intercept and slope. (Ch). The slope differed significantly between the sites

To achieve this, 1000 bootstrap sample pairs (each pair for DBH versus Cd, with greater slope found for NOlinda encompassing all 65 trees) were drawn in order to obtain (Figure 2d). Both slope and the intercept differed between the null distribution of no difference between sites (i.e, H0: sites for the relationship between Cd and Ht, with greater Apuí - NOlinda = 0). The probability p for rejection of intercept and lower slope for Apuí (Figure 2e).

H0 was obtained by the proportion of cases in which the There was a significant difference in stem form factor observed differences of the intercepts and slopes between (FF) between sites (t = 2.66, p = 0.01, GL = 63). The FF in Apuí and NOlinda were smaller than 0.05. In other words, Apuí (0.83 ± 0.082, mean ± standard deviation) averaged the observed difference was large enough to state that it 7.8% higher than in NOlinda (0.77 ± 0.079). Volume fitted was not due to chance alone. as a function of DBH was highly significant for both sites Exponential nonlinear models were tested to determine (Apuí: r2 = 99.7%; NOlinda: r2 = 96.5%, p <0.0001 for the relationship between tree size (DBH) and wood density both cases, Table 1), and the model parameters differed for each site separately. Two-way analysis of variance was significantly, with both greater slope and intercept for used to test the effects on wood density of site and of the Apuí (Table 1, Figure 2f). position of the cross section along the length of the bole. 3.2. Wood density The effect of position in this analysis was calculated for three positions: 1.30 m (the DBH measurement point), There was a significant positive relationship between

50% (the midpoint of the bole) and the top of the bole. DBH and wood density (F1,64 = 10.48, p = 0.001) for Apuí, Because it is not appropriate to assume that samples are for which DBH explained 35.8% of the variation in wood independent within the same bole, we randomly selected density. On the other hand, no significant relationship was different trees to obtain the wood density of each bole found for NOlinda (F1,64 = 0.63, p = 0.403, Figure 3). position within each site. ANOVA detected a highly significant site effect on wood

density (F1,64 = 38.88, p < 0.001). Wood density in NOlinda 3. Results (0.74 ± 0.033, mean ± standard deviation) was, on average, 8.8% higher than in Apuí (0.68 ± 0.042). The position 3.1. Allometry of the sample in the bole also influenced wood density

All linear regressions for DBH versus the other variables (F2,64 = 4.82, p = 0.012), with the wood density at 1.30 m

(Hs, Ht, Ch, and Cd) were significant, except log10 (DBH) differed significantly from that at the top of the bole versus log10 (Ch) for Apuí (Table 1, Figure 2a). There was (p = 0.009, Tukey test). Wood density decreased from

Table 1. Regression coefficients, bootstrapped 95% confidence intervals (LL = lower limit and UL= upper limit)and probabilities (p) associated with the rejection of the null hypothesis of no difference between coefficients related to forest sites calculated by bootstrapping. Probabilities in bold denote significant differences between sites at p < 0.05. Bootstrapped 95% confidence Allometric Forest Coefficients intervals p r2 relationships Intercept Slope site Intercept Slope LL UL LL UL Intercept Slope Apuí 16.22 0.20 0.44 12.04 21.02 0.09 0.31 DBH vs. H 0.53 0.71 t NOlinda 17.44 0.22 0.67 15.04 20.16 0.17 0.27 Apuí 0.19 0.54 0.57 –0.08 0.49 0.36 0.69 log DBH vs. log H 0.002 0.002 s NOlinda 0.61 0.29 0.28 0.44 0.78 0.19 0.39 Apuí 0.87 0.14 0.02 0.47 1.34 –0.17 0.42 log DBH vs. log C 0.051 0.03 h NOlinda 0.52 0.39 0.46 0.37 0.75 0.26 0.49 Apuí 3.87 0.19 0.80 2.3 5.8 0.15 0.22 DBH vs. C 0.47 0.007 d NOlinda 3.2 0.25 0.89 0.32 4.32 0.22 0.3 Apuí 1.42 0.45 0.39 –3.58 7.52 0.24 0.64 H vs. C 0.024 0.015 t d NOlinda –5.73 0.74 0.55 –16.12 –0.44 0.56 1.1 Apuí –3.94 2.49 0.98 –4.16 –3.68 2.33 2.62 log DBH vs. log V 0.003 0.003 NOlinda –3.59 2.27 0.97 –3.78 –3.42 2.16 2.37

Braz. J. Biol., 2016, vol. 76, no. 1, pp. 268-276 271 Siliprandi, N.C. et al.

Figure 2. Regression models fitted to data on DBH versus (a) Ht, (b) Hs, (c) Ch and (d) Cd, (e) Ht versus Cd and (f) DBH versus Vc. Regressions of DBH with Hs and Ch are log10-transformed for both axes. Regression coefficients are shown in Table 1.

the base to the top of the bole, with the pooled average for both sites being 0.74, 0.71 and 0.70 g cm-3 at 1.30 m, middle and at the top of the bole, respectively (Figure 4).

4. Discussion Our findings suggest that the allometry of G. glabra significantly differed between sites, especially regarding to the relationships of crown shape to DBH and height. These differences mirror the interspecific allometric variations within the same site in terms of adult stature (canopy/emerging species versus understory species) Figure 3. Relationship between DBH and wood density for and/or demand for light (pioneer versus shade tolerant trees at each forest site. species) (e.g., King, 1996; Sterck and Bongers, 1998;

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Bongers, 2001). However, the opposite phyllotaxis and the small of G. glabra can minimize the effect of canopy shading. In this case, the increase in canopy height could result in an increase in the number of layers of leaves and, by inference, the specific area. Rather, the better light conditions experienced by trees in Apuí means that they do not need to invest large amounts of resources in increasing photosynthetic area. A deep and wide canopy does not necessarily imply a greater number of leaf layers, but the distribution and geometry (shape, size and orientation) of foliage can play a crucial role in the light interception (Poorter et al., 2006). Allometric differences in this study corroborate the Figure 4. Mean (± standard deviation) of wood density at variation in wood density between sites. Wood density is different stem positions for each forest site. directly related to mechanical structure, and by inference, the ability of a tree to support its own weight and to resist Poorter et al., 2006). Thus, the allometric differences found exogenous forces, such as wind and pushing over by in this study can be attributed to abiotic differences related other trees (King, 1981; Putz et al., 1983; Chave et al., mainly to the quantity and quality of light reaching the 2009). However, recent studies have cast doubt on these understory, as well as the variation in soil physical and ideas, showing that the same strength for supporting tree chemical characteristics between sites. weight is achieved by a trunk with low wood density (with lower construction cost) than by one with higher Tree architecture within the same species may vary wood density (Anten and Schieving, 2010). Larjavaara during ontogeny and depends on abiotic conditions (mainly and Muller-Landau (2010) proposed that species with light availability) in which individual trees grow. Rapid low wood density, such as pioneers, prioritize short-term changes in the development of the crown may occur gains over long-term costs, thereby not only evolving low when a tree reaches the canopy due to an increase in wood density, but also low trunk and xylem resistance. light exposure (King and Maindonald, 1999; Sterck and Low light levels may induce tropical trees to reduce their Bongers, 2001; Osunkoya et al., 2007). Although G. glabra diameter growth, thus resulting in higher wood density trees had similar H at both sites, this was not true for the t (Thomas, 1996). This also results in a greater investment relationship between DBH and H , indicating that trees in s in vertical growth and crown expansion at the expenses of NOlinda invest more in stem elongation in the smaller size stem thickness (Sterck et al., 2001; Osunkoya et al., 2007; classes, but for larger trees the opposite pattern occurs: trees Poorter et al., 2006). A thinner trunk with high wood density in Apuí invest more in stem elongation throughout tree is more flexible than a thicker one with low wood density ontogeny, which resulted in significantly higher regression and equal strength, and flexibility can be advantageous slope and lower intercept at this site. Such high initial in reducing sail area during short gusts of wind and in stem growth in NOlinda can be attributed to the fact that allowing the tree to bounce back after having been struck a tree growing in dense rain forest, where it is assumed by falling trees or branches. In this sense, the greater that light incidence is lower when compared to the open crown expansion of G. glabra in NOlinda required more forest in Apuí, needs to invest more in vertical growth at investment in strength and flexibility, and thus in higher this stage to increase access to light. wood density. In a rainforest in Borneo, Osunkoya et al. The differences in growth in Cd and Ch corroborate the (2007) showed that the safety factor (a measure related reduced growth found for Hs (in the initial phase) for trees directly to physical properties of the wood) had strong in NOlinda, where they invest less in Ch and Cd, but have positive relationships with crown diameter and depth, deeper and wider crowns when fully developed. In Apuí indicating that trees (regardless of species) with greater the relationship between DBH and Ch was not significant, horizontal or vertical crown expansion had higher safety indicating that Ch remains constant after stems reach a margins against rupture (see also King, 1996; Sterck and certain height, at least for trees ≥ 10 cm DBH. Because Bongers, 1998; Alves and Santos, 2002). low light intensity implies a lower photosynthetic rate, The difference in taper between sites may also represent perhaps it is a better strategy for a species growing in the an adaptive strategy in terms of mechanical support because dense rainforest to invest energy in early height growth to the increase in the stem base may improve support and reach the canopy rapidly and, in later stages, to increase fixation Sposito( and Santos, 2001). A larger taper in specific leaf area by expanding the canopy to intercept NOlinda can be related to decreasing risk of deflection a larger quantity of light. In fact, the variation in bole of the stem as a result of the greater weight generated by volume between sites is a consequence of differences in the crown expansion. Therefore, we concluded that there taper (form factor) and Hs during ontogeny. are different adaptive strategies during the ontogeny of Increasing canopy height may result in higher self‑shading G. glabra acting on resource allocation and occupation of of the leaves due to the packing of leaf layers (Sterck and space mainly as a result of differences in light availability

Braz. J. Biol., 2016, vol. 76, no. 1, pp. 268-276 273 Siliprandi, N.C. et al. between sites. NOlinda trees need to invest heavily in 5. Conclusions initial height growth by allocating more carbon per unit At the community level, allometric differences have volume of stem in this phase, so that an increase in the been found in trees in different forest types in Amazonia safety margin against breakage may be achieved when and in other tropical forests (Nogueira et al., 2008a; trees reach the canopy and start investing more in crown Feldpausch et al., 2011; Banin et al., 2012). The results of expansion. In contrast, trees in Apuí allocate less carbon the present study are unique because they show differences per unit volume of stem during their ontogeny, as canopy in allometric relations and in wood density for the same expansion is significantly lower than in NOlinda. In fact, species growing in two forest types in Brazilian Amazonia. the non-significant relationship between DBH and wood These allometric differences have implications for biomass density for NOlinda and the positive relationship for Apuí estimates for this species and represent a warning of one (Figure 4) demonstrate that carbon allocation to stems in more possible bias in biomass estimates generally when NOlinda occurs equally throughout ontogeny, whereas for obtained by means of allometric equations. This even applies trees in Apuí the allocation of biomass changes as the tree to those equations that include both tree height and wood grows, with an increase occurring at the end of ontogeny density as explanatory variables but assume no differences when horizontal crown expansion starts. in crown biomass. In the present study, the biomass of Among tropical tree species, tree growth is negatively Goupia glabra will be higher at the NOlinda site (central related to wood density (Thomas, 1996; Muller-Landau, 2004; Amazonia) than at the Apuí site (southern Amazonia) due Nascimento et al., 2005; King et al., 2006). In addition, within both to denser wood in all trees (Figure 3) and to larger the same species wood density is higher in slow‑growing crowns in the case of the trees with large diameters and trees than in fast-growing trees (Koubaa et al., 2000), heights (Figure 3d, e). These height and density differences indicating that G. glabra may have faster growth in Apuí between central and southern Amazonia are consistent and, as a result, there must be a difference between sites with the pattern for species studied by Nogueira et al. in the age of trees of same diameter. However, such a (2007, 2008a, b). difference should be evaluated empirically, and we suggest this approach for future studies. The distribution of life-history strategies, and particularly Acknowledgements the wood density of tropical tree species, may vary among sites depending on environmental features such as climate This contribution is part of the first author’s Master thesis undertaken at the National Institute of Amazonian Research periodicity, soil conditions, disturbance regimes and (INPA), with fellowships from the Amazonas Research competition for light (Muller-Landau, 2004; Nogueira et al., Foundation (FAPEAM, process #143643/2008‑8). We are 2007; Patiño et al., 2009). Sites with high disturbance grateful to the landowners, Antonio M. R. de Arrunda, regimes on relatively fertile soils may favor fast-growing Raimundo de S. Maia Filho, Sergio S. Souza (Fazenda species that have low wood density, while sites with lower Apapazinho) and Marcos V. Conceicao (Fazenda Nova frequencies of disturbance and with nutrient-poor soils Era) who provided us financial and logistic support for reduce tree growth (Baker et al., 2004; Muller-Landau, fieldwork. Our special thanks to Antonio Siliprandi, Norian 2004). Patiño et al. (2009) have shown that branch xylem C. Siliprandi, Nivaldo Carline, Ivone C. Siliprandi Michele density varies considerably across Amazonia, and that Gusmao, Susy D. Souza, Manoel J.F. Mar, Pedro S. Silva 33% and 26% of this variation is attributable to phylogeny and Joaquim G. Silva for assistance in the field. and environmental factors, respectively. The remaining 41% is attributable to intraspecific differences related to phenotypic plasticity in many tree species. References In the present study, the difference in wood density ALVES, L.F. and SANTOS, F.A.M., 2002. Tree allometry and between sites is a straightforward consequence of crown shape of four tree species in Atlantic rain forest, southeast the phenotypic plasticity of G. glabra in response to Brazil. Journal of Tropical Ecology, vol. 18, no. 2, pp. 245-260. different environmental conditions. In seasonally flooded http://dx.doi.org/10.1017/S026646740200216X. várzea (white water floodplain) forests in the Amazon, AMERICAN SOCIETY FOR TESTING AND MATERIALS Wittmann et al. (2006) attributed the differences in wood – ASTM, 2002. Standard test methods for specific gravity of density of two tree species, Tabebuia barbata and Hevea wood and wood-based materials. Designation: D 2395-02. spruceana, to the level and duration of flooding, which Pennsylvania: ASTM. 75 p. leads to different water conditions and, consequently, to ANTEN, N.P. and SCHIEVING, F., 2010. The role of wood the reduction of tree growth during the aquatic phase, i.e., mass density and mechanical constraints in the economy of tree sites with higher levels and durations of flooding result in architecture. American Naturalist, vol. 175, no. 2, pp. 250-260. greater physiological stress that decreases tree growth and http://dx.doi.org/10.1086/649581. PMid:20028240. increases wood density. In the present study, differences BAKER, T.R., PHILLIPS, O.L., MALHI, Y., ALMEIDA, S., in soil fertility and disturbance regimes between Apuí ARROYO, L., DI FIORE, A., ERWIN, T., KILLEEN, T.J., and NOlinda can also be considered as crucial factors for LAURANCE, S.G., LAURANCE, W.F., LEWIS, S.L., LLOYD, different strategies of G. glabra growth, and the subject J., MONTEAGUDO, A., NEILL, D.A., PATIÑO, S., PITMAN, is appropriate for future studies. N.C.A., SILVA, J.N.M. and MARTÍNEZ, J.V., 2004. Variation

274 Braz. J. Biol., 2016, vol. 76, no. 1, pp. 268-276 Allometry of an Amazonian tree species in wood density determines spatial patterns in Amazonian forest KING, D.A., 1996. The allometry and life history of tropical biomass. Global Change Biology, vol. 10, no. 5, pp. 545-562. trees. Journal of Tropical Ecology, vol. 12, no. 1, pp. 25-44. http://dx.doi.org/10.1111/j.1365-2486.2004.00751.x. http://dx.doi.org/10.1017/S0266467400009299. BANIN, L., FELDPAUSCH, T.R., PHILLIPS, O.L., BAKER, KING, D.A., DAVIES, S.J., TAN, S. and NOOR, N.S.M., 2006. T.R., LLOYD, J., AFFUM-BAFFOE, K., ARETS, E.J.M.M., The role of wood density and stem support costs in the growth BERRY, N.J., BRADFORD, M., BRIENEN, R.J.W., DAVIES, S., and mortality of tropical trees. Journal of Ecology, vol. 94, no. 3, DRESCHER, M., HIGUCHI, N., HILBERT, D.W., HLADIK, A., pp. 670-680. http://dx.doi.org/10.1111/j.1365-2745.2006.01112.x. IIDA, Y., SALIM, K.A., KASSIM, A.R., KING, D.A., LOPEZ- KOUBAA, A., ZHANG, S.Y., ISABEL, N., BEAULIEU, J. and GONZALEZ, G., METCALFE, D., NILUS, R., PEH, K.S.-H., BOUSQUET, J., 2000. Phenotypic correlations between juvenile REITSMA, J.M., SONKÉ, B., TAEDOUMG, H., TAN, S., WHITE, mature wood density and growth in black spruce. Wood and Fiber L., WÖLL, H. and LEWIS, S.L., 2012. What controls tropical Science, vol. 32, no. 1, pp. 61-71. forest architecture? Testing environmental, structural and floristic drivers. Global Ecology and Biogeography, vol. 21, no. 12, pp. LARJAVAARA, M. and MULLER-LANDAU, H.C., 2010. Rethinking the value of high wood density. Functional Ecology, 1179-1190. http://dx.doi.org/10.1111/j.1466-8238.2012.00778.x. vol. 24, no. 4, pp. 701-705. http://dx.doi.org/10.1111/j.1365- BOOT, R.G.A., 1996. The significance of seedling size and growth 2435.2010.01698.x. rate of tropical forest tree seedlings for regeneration in canopy LOUREIRO, A., SILVA, M.F. and ALENCAR, J.C., 1979. openings. In: M.D. SWAINE, ed. The ecology of tropical forest Essências madeireiras da Amazônia. Manaus: SUFRAMA. 432 p. tree seedlings. Paris: UNESCO. pp. 267-284. MAS UNESCO Series, Vol. 17. MULLER-LANDAU, H.C., 2004. Interspecific and inter-site variation in wood specific gravity of tropical trees. Biotropica, CHAVE, J., COOMES, D., JANSEN, S., LEWIS, S., SWENSON, vol. 36, no. 1, pp. 20-32. N.G. and ZANNE, A.E., 2009. Towards a worldwide wood economics spectrum. Ecology Letters, vol. 12, no. 4, pp. 351-366. http:// NASCIMENTO, H.E.M., LAURANCE, W.F., CONDIT, R., dx.doi.org/10.1111/j.1461-0248.2009.01285.x. PMid:19243406. LAURANCE, S.G., D’ANGELO, S. and ANDRADE, A.C., 2005. Demographic and life-history correlates for Amazonian CHAZDON, R.L. and FETCHER, N., 1984. Photosynthetic trees. Journal of Vegetation Science, vol. 16, no. 6, pp. 625-634. light environments in a lowland tropical rainforest in Costa Rica. http://dx.doi.org/10.1111/j.1654-1103.2005.tb02405.x. Journal of Ecology, vol. 72, no. 3, pp. 552-564. NIKLAS, K.J., 1993. Influence of tissue density-specific mechanical EFRON, B. and TIBSHIRANI, R.J., 1993. An introduction to the properties on the scaling of height. Annals of Botany, vol. bootstrap. New York: Chapman & Hall. 456 p. 72, no. 3, pp. 173-179. FELDPAUSCH, T.R., BANIN, L., PJILLIPS, O.L., BAKER, NOGUEIRA, E.M., FEARNSIDE, P.M., NELSON, B.W. and T.R., LEWIS, S.L., QUESADA, C.A., AFFUM-BAFFOE, K., FRANÇA, M.B., 2007. Wood density in forests of Brazil’s arc of ARETS, E.J.M.M., BERRY, N.J., , M., BRONDIZIO, E.S., deforestation: implications for biomass and flux of carbon from CAMARGO, P., CHAVE, J., DIAGBLETEY, G., DOMINGUES, land-use change in Amazonia. Forest Ecology and Management, T.F., DRESCHER, M., FEARNSIDE, P.M., FRANÇA, M.B., vol. 248, no. 3, pp. 119-135. http://dx.doi.org/10.1016/j. FYLLAS, N.M., LOPEZ-GONZALEZ, G., HLADIK, A., HIGUSHI, foreco.2007.04.047. N., HUNTER, M.O., IIDA, Y., SALIM, K.A., KASSIM, A.R., NOGUEIRA, E.M., NELSON, B.W., FEARNSIDE, P.M., KELLER, M., KEMP, J., KING, D.A., LOVETT, J.C., MARIMON, FRANÇA, M.B. and OLIVEIRA, A.C.A., 2008a. Tree height B.S., MARIMON-JUNIOR, B.H., LENZA, E., MARSHALL, in Brazil’s ‘arc of deforestation’: shorter trees in south and A.R., METCALFE, D.J., MITCHARD, E.T.A., MORAN, E.F., southwest Amazonia imply lower biomass. Forest Ecology NELSON, B.W., NILUS, R., NOGUEIRA, E.M., PALACE, and Management, vol. 255, no. 7, pp. 2963-2972. http://dx.doi. M., PATIÑO, S., PEH, K.S.-H., RAVENTOS, M.T., REITSMA, org/10.1016/j.foreco.2008.02.002. J.M., SAIZ, G., SCHRODT, F., SONKÉ, B., TAEDOUMG, H.E., OSUNKOYA, O.O., OMAR-ALI, K., AMIT, N., DAYAN, J., TAN, S., WHITE, L., WÖLL, H. and LLOYD, J., 2011. Height- DAUD, D.S. and SHENG, T.K., 2007. Comparative height– diameter allometry of tropical forest trees. Biogeosciences, vol. 8, crown allometry and mechanical design in 22 tree species of no. 5, pp. 1081-1106. http://dx.doi.org/10.5194/bg-8-1081-2011 Kuala Belalong rainforest, Brunei, Borneo. American Journal of FERREIRA, L.M.M. and TONINI, H., 2004. Cupiúba (Goupia Botany, vol. 94, no. 12, pp. 1951-1962. http://dx.doi.org/10.3732/ glabra Aublet): crescimento, potencialidades e usos. Boa Vista: ajb.94.12.1951. PMid:21636390. Embrapa Roraima. 27 p. Documentos, no. 4. PATIÑO, S., LLOYD, J., PAIVA, R., BAKER, T.R., QUESADA, INSTITUTO NACIONAL DE METEOROLOGIA – INMET, C.A., MERCADO, L.M., SCHMERLER, J., SCHWARZ, M., SANTOS, A.J.B., AGUILAR, A., CZIMCZIK, C.I., GALLO, J., 2009 [viewed 5 June 2013]. Normais Climatológicas do Brasil HORNA, V., HOYOS, E.J., JIMENEZ, E.M., PALOMINO, W., 1961-1990. Brasília. IMET [online]. Available from: http://www. PEACOCK, J., PEÑA-CRUZ, A., SARMIENTO, C., SOTA, A., inmet.gov.br/portal/index.php?r=clima/normaisclimatologicas TURRIAGO, J.D., VILLANUEVA, B., VITZTHUM, P., ALVAREZ, KING, D.A. and MAINDONALD, J.H., 1999. Tree architecture E., ARROYO, L., BARALOTO, C., BONAL, D., CHAVE, J., in relations to leaf dimensions and tree stature in temperate COSTA, A.C.L., HERRERA, R., HIGUCHI, N., KILLEEN, T., and tropical rain forests. Journal of Ecology, vol. 87, no. 6, pp. LEAL, E., LUIZÃO, F., MEIR, P., MONTEAGUDO, A., NEIL, D., 1012-1024. http://dx.doi.org/10.1046/j.1365-2745.1999.00417.x. NÚÑEZ-VARGAS, P., PEÑUELA, M.C., PITMAN, N., PRIANTE FILHO, N., PRIETO, A., PANFIL, S.N., RUDAS, A., SALOMÃO, KING, D.A., 1981. Tree dimensions: maximizing the rate of height R., SILVA, N., SILVEIRA, M., SOARES DEALMEIDA, S., growth in dense stands. Oecologia, vol. 51, no. 2, pp. 351-356. TORRES-LEZAMA, A., VÁSQUEZ-MARTÍNEZ, R., VIEIRA, http://dx.doi.org/10.1007/BF00540905. I., MALHI, Y. and PHILLIPS, O.L., 2009. Branch xylem density

Braz. J. Biol., 2016, vol. 76, no. 1, pp. 268-276 275 Siliprandi, N.C. et al. variations across the Amazon Basin. Biogeosciences, vol. 6, no. American Journal of Botany, vol. 88, no. 5, pp. 939-949. http:// 4, pp. 545-568. http://dx.doi.org/10.5194/bg-6-545-2009. dx.doi.org/10.2307/2657047. PMid:11353719. POORTER, L., BONGERS, L. and BONGERS, F., 2006. STERCK, F.J. and BONGERS, F., 1998. Ontogenetic changes Architecture of 54 moist-forest tree species: traits, trade-offs, in size, allometry, and mechanical design of tropical rain forest and functional groups. Ecology, vol. 87, no. 5, pp. 1289-1301. trees. American Journal of Botany, vol. 85, no. 2, pp. 266-272. http://dx.doi.org/10.1890/0012-9658(2006)87[1289:AOMTST] http://dx.doi.org/10.2307/2446315. PMid:21684910. 2.0.CO;2. PMid:16761607. STERCK, F.J. and BONGERS, F., 2001. Crown development PUTZ, F.E., COLEY, P.D., LU, K., MONTALVO, A. and in tropical rain forest trees: patterns with tree height and light AIELLO, A., 1983. Uprooting and snapping of trees: structural availability. Journal of Ecology, vol. 89, no. 1, pp. 1-13. http:// determinants and ecological consequences. Canadian Journal dx.doi.org/10.1046/j.1365-2745.2001.00525.x. of Forest Research, vol. 3, no. 5, pp. 1011-1020. http://dx.doi. org/10.1139/x83-133. STERCK, F.J., BONGERS, F. and NEWBERY, D.M., 2001. Tree architecture in a Bornean lowland rainforest: intraspecific and RIBEIRO, J.E.L., HOPKINS, M.J.G., VICENTINI, A., SOTHERS, interspecific patterns. Plant Ecology, vol. 153, no. 1, pp. 279-292. C.A., COSTA, M.A.S., BRITO, J.M., SOUZA, M.A.D., MARTINS, http://dx.doi.org/10.1023/A:1017507723365. L.H.P., LOHMAN, L.G., ASSUNÇÃO, P.A.C.L., PEREIRA, E.C., SILVA, C.F., MESQUISTA, M.R. and PROCÓPIO, L.C., SWAINE, M. and WHITMORE, T.C., 1988. On definition of 1999. Flora da Reserva Ducke: guia de identificação das plantas ecological species groups in tropical rain forests. Vegetatio, vol. vasculares de uma floresta de terra-firme na Amazônia Central. 75, no. 1, pp. 81-86. http://dx.doi.org/10.1007/BF00044629. Manaus: INPA. 816 p. SWENSON, N.G. and ENQUIST, B.J., 2007. Ecological and SANTOS, H.G., CARVALHO JÚNIOR, W., DART, R.O., evolutionary determinants of a key plant functional trait: wood ÁGLIO, M.L.D., SOUZA, J.S., PARES, J.G. and FONTANA, density and its community wide variation across latitude and A., MARTINS, A.L.S. and OLIVEIRA, A.P., 2011. O novo mapa elevation. American Journal of Botany, vol. 94, no. 3, pp. 451- de solos do Brasil: legenda atualizada. 2nd ed. Rio de Janeiro: 459. http://dx.doi.org/10.3732/ajb.94.3.451. PMid:21636415. Embrapa Solos. 67 p. Documentos, no. 130. THOMAS, S.C., 1996. Asymptotic height as a predictor of SLIK, J.W.F., AIBA, S.-I., BREARLEY, F.Q., CANNON, C.H., growth and allometric characteristics in Malaysian rain forest FORSHED, O., KITAYAMA, K., NAGAMASU, H., NILUS, R., trees. American Journal of Botany, vol. 83, no. 5, p. 556-566. PAYNE, J., PAOLI, G., POULSEN, A.D., RAES, N., SHEIL, D., SIDIYASA, K., SUZUKI, E. and VAN VALKENBURG, J.L.C.H., WIEMANN, M.C. and WILLIAMSON, G.B., 2002. Geographic 2010. Environmental correlates of tree biomass, basal area, wood variation in wood specific gravity: effects of latitude, temperature, specific gravity and stem density gradients in Borneo’s tropical and precipitation. Wood and Fiber Science, vol. 34, no. 1, pp. 96-107. forests. Global Ecology and Biogeography, vol. 19, no. 1, pp. WITTMANN, F., SCHÖNGART, J., PAROLIN, P., WORBES, 50-60. http://dx.doi.org/10.1111/j.1466-8238.2009.00489.x. M., PIEDADE, M.T.F. and JUNK, W.J., 2006. Wood specific SPOSITO, T.C. and SANTOS, F.A.M., 2001. Scaling of stem gravity of trees in Amazonian white-water forests in relation to and crown in eight Cecropia (Cecropiaceae) species of Brazil. flooding. IAWA Journal, vol. 27, no. 3, pp. 255-268.

276 Braz. J. Biol., 2016, vol. 76, no. 1, pp. 268-276